Fruit Growth and Dry Matter Accumulation in Grapefruit during Periods of Water Withholding and after Reirrigation*
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1 Aust. J. Plant Physiol., 1988, 15, Fruit Growth and Dry Matter Accumulation in Grapefruit during Periods of Water Withholding and after Reirrigation* Aharon Cohen and Ari Goell Department of Citriculture, Agricultural Research Organization, The Volcani Center, Bet Dagan 50250, Israel. Abstract Changes in volume, fresh weight and dry matter (DM) contents were followed in fruits from girdled and non-girdled branches borne on regularly irrigated (RI) as well as water-stressed (S) trees. Water stress was imposed by withholding irrigation for various periods. The results indicate that, even during prolonged periods of drought, DM accumulation in fruits on S trees was only slightly impaired, even when fruit volume growth was reduced to zero or even to shrinkage. After irrigation was resumed, fruits from S trees grew faster than those from RI trees, indicating that some of the DM which had accumulated was available for volume growth. The possibility of using the rate of DM accumulation in the fruit as an indicator for the timing of irrigation is discussed. Introduction Fruits from citrus trees subjected to drought periods by withholding irrigation (WI) grew at a faster rate after irrigation than did fruits from regularly irrigated (RI) trees (Furr and Taylor 1939; Oppenheimer and Elze 1941; Goell et al. 1981). Similar results have been reported for peaches (Chalmers and Wilson 1978), and pears (Chalmers et al. 1986; Mitchell et al. 1986). The faster growth rate occurred not only during the first cycle after termination of the WI period, but continued during later irrigation cycles, sometimes lasting 4-6 weeks (Cohen and Goell 1984), suggesting that the factor responsible for the faster growth was non-labile. Juice from fruits borne on trees that had been subjected to prolonged periods of water stress during the summer contained higher levels of acidity and total soluble solids (TSS) at harvest, than did the juice of fruits from RI trees (Goell and Levy 1970; Goell 1972). This may have resulted from enhanced metabolic processes (Yelenosky 1978; McNulty 1985), or from the accumulation of dry matter (DM) during the water-stressed (S) period which was not completely utilised for volume growth of the fruit even after irrigation was resumed. Some of the accumulated photosynthates might, however, be available for the extra, rapid fruit growth reported for the period after S has been terminated. Accumulation of DM in S fruits at a rate similar to that in RI trees may be the result of continued, near-normal levels of photosynthesis during the stress period, or the expression of a withdrawal of photosynthates from reserves existing in the tree. The study of fruits on girdled branches bearing a fixed number of leaves per fruit (Cohen 1984) can help determine which of the above possibilities occurs. This study was undertaken to investigate the changes in the growth rate and DM contents of fruits on girdled and non-girdled branches during a drought (WI) period, as well as during the period following the resumption of irrigation. *Contribution from the Agricultural Research Organization, The Volcani Center, Bet Dagan, No E, 1987 series / 88/050633$03.00
2 Aharon Cohen and Ari Goell Materials and Methods Field trials were carried out during the years 1983 and 1984 on mature (20-25 years) 'Marsh Seedless' grapefruit (C. paradisi Macf.) trees, or Sour Orange stock, growing in several orchards of the Volcani Center at Bet Dagan (BD), and at Beror Hayil (BH), in the southern coastal plain of Israel. Planting distances were 6 x 4 m. The soil was a sandy-loam to loam at BD and a clay loam at BH. The treatments were applied to single or double rows of 6-10 trees each, with no buffer rows between treatments (Goell and Cohen 1981). Irrigation was by means of solid-set plastic pipes laid along the trunk line, with one 70 1/ h microjet ('Ein Tal' Series 70) per tree. Intervals and applications were those considered standard for the region. In the summer, these were 7-14 days between applications of 4 mm (96 litres per tree) per day. Irrigation stress was arrived at in the S trees by withholding irrigation (WI) for various periods in the summer and fall, i.e. omitting two or more scheduled (RI) irrigations. Irrigation was resumed at the RI level in the BH 1983 and 1984 trials, while in the BD trials an extra 25% was given in the first two applications after WI was terminated. Only one tfhl (BD 1983) was considered to have been fully rewetted, after a late season WI period was terminated by early rains. The actual period of stress in the S treatments was calculated by subtracting one normal RI interval from the total number of days of WI. All other orchard operations continued regularly, with fertiliser being broadcast by hand onto the soil area wet by the microjets. Fruit Measurements All the fruits for the periodic samplings were tagged on 6-10 trees in each replication after 'June drop'. Fruits were chosen for uniformity in initial circumference measurements, and circumference growth was followed throughout the experimental period, including the period between the irrigation terminating the WI period and harvest. Actual fruit volume, determined on all sampled fruits using a specially adapted floater method (Cohen et al. 1968), was highly correlated (?= ) with the volume calculated according to Turrell(1946). The changes reported for volume of fruit on the trees are based on the calculuted volume, as derived from fruit samples on each date. The DM contents of sampled fruits were determined after 7 days in a forced-draft oven at 75 C. Dry matter per unit volume (mg DM/cm3) of the fruit was calculated from the sampled fruits at each sampling date, and was used to calculate the DM contents of the tagged fruits remaining on the tree. In 1984, two separate groups of fruit - borne on girdled and non-girdled branches - were tagged and measured on the same treatment trees in the manner described. Both groups were chosen to make the leaf/fruit ratio and the initial fruit size as uniform as possible. The girdled branches (girdle width = 20 mm) bore 40 leaves per fruit above the girdle (Cohen 1984) while the other fruits were borne on similar, ungirdled branches. Results and Discussion The effects of various drought periods on the changes in fresh weight, volume and DM content for fruits from S trees, relative to changes in RI fruits are presented in Table 1. In all trials the effects of the drought periods on volume growth were more pronounced than those on fresh weight. The accumulation of DM in the fruits from the S trees during the WI period was affected much less than either fresh weight or fruit volume. In three of the trials (Nos 5, 6 and 1 I), even though the S fruits actually shrank in volume, they accumulated DM at a rate similar to that in fruits from RI trees. The increase in DM content in the S fruits could be expressed on the basis of fresh weight or volume. In the following tables, results will be presented as DM/volume, since it was felt that volume relates better to the fruit growth rate. Table 2 presents values for DM/unit fruit volume only for those trials at BD in which fruit volume loss (shrinkage) occurred during the drought period (trials 3-7). In addition to the data on the DM/unit volume contents of the S and RI fruits at
3 Water Stress, Fruit Growth and Dry Matter in Grapefruit Table 1. Effect of various drought periods on changes in fresh weight, volume and DM accumulation during the WI period Data are expressed as the increments in S fruits as % of those in RI fruits. Duration of S = days during which water was withheld, less one RI interval. Values for Trials 1 and 2 are averages for 40 fruits; all the rest are averages from samples of fruits Year Trial Irrigation S GirdlingA Relative change (% S 1 RI) No. interval Period Days Fresh Fruit DM (days) wt vol, accum. Aug. Aug.-Sept. July-Aug. Aug. Aug.-Sept. Bet Dagan 39 N 58 N Beror Hayil 55 N 55 G 11 ~ o s s ~ 18 Loss 26 Loss 22 Loss 22 Loss Loss *N = non-girdled branches, G = girdled branches. B~hrinkage fruit volume. Table 2. Mean 2 s.e. DM per unit fruit volume (mg/cm3) for fruits from RI and S fruits sampled at the end of the WI period, and the levels of 'excess DM' calculated for S fruits at this stage from volume ( Vs) and DMs 'Excess' DM per fruit was defined as the amount of DM that had accumulated in the fruit during the drought period which did not contribute to fruit volume growth. For mode of calculation see text. Details of trials and sample size as in Table 1 Trial DM 1 unit volume (mg l em3) VS at Excess DM No. RI S reirrig. in S fruits (em3) (g/ fruit) f f f the end of the WI period, calculations were made of excess DM/S fruit - defined as the amount of DM accumulating in a fruit during the drought period in excess of that accumulating in an RI fruit. Calculations were made as follows: Es = Vs (Ds - DRI) where ES = excess DM per S fruit, VS = S fruit volume, and DS and DRI = mg DM/ cm3 fruit volume for S and RI fruits, respectively.
4 Aharon Cohen and Ari Goell From Table 2 it can be seen that there were large amounts of excess DM in the S fruits, enough to have added cm3 to fruit volume, if they had been utilised as in the RI fruits. Table 3 presents data on fruit volume growth and DM accumulation in S fruits, relative to RI fruits, during the period between resumption of irrigation and harvest of the fruits. In all five trials, volume increase of the S fruits was greater than that in RI. This faster growth rate of the S fruits was found to continue even after the turgor-attributed, initial swelling stage of fruit growth had been completed. In trials 3 and 4, for example, periodic measurements showed that for S fruits the growth rate from day 8 after irri- Table 3. The relative increment in fruit volume and DM contents in S fruits, for the period between reirrigation and harvest, as VO of those for RI fruits During this period all trials received water as RI, plus 25% of the withheld water, applied in the first 2 irrigations. Bet Dagan trials, Trial details and fruit sampling as in Table 1 Trial ~irdling~ Period between irrigation Relative increment (% S/RI) No. renewal and harvest Fruit vol. DM N 19 Au~ Oct N 3 Sept Oct G 8 Aug. - 3 Sept G 19 Aug Oct G 3 Sept Oct AN = non-girdled branches, G = girdled branches. Table 4. Mean 2 s.e. DM/unit volume (mg/cm3) in fruits from RI and S trees for the period between reirrigation and hamest Trial details and fruit sampling number same as for Table 1 Trial GirdlingA Harvest Days after DM/ unit volume (mg /cm3) "70 No. date reirrigation RI S S/RI 3 N 30 Oct N 30 Oct G 3 Sept G 30 Oct G 30 Oct A~ = non-girdled branches, G = girdled branches. gation was resumed until harvest was 32 and 24% higher, respectively, than in the corresponding RI fruits. This faster growth rate cannot be attributed to the differences in the amounts of irrigation applied after drought, since such faster growth occurred also in trial 2, in which both treatments were rewetted equally by rains only (see Materials and Methods). The indication is, therefore, that at least part of the volume increase in the fruits after irrigation renewal was due to factors other than turgor adjustment at the higher water potential. During the period following WI, DM accumulated faster in the S fruits from girdled branches than in those from non-girdled ones. This may have been due to the fact that fruits from girdled branches did not have to compete with other sinks in the tree, as fruits from non-girdled branches do. Such faster accumulation could also have been the
5 Water Stress, Fruit Growth and Dry Matter in Grapefruit 637 result of the fact that the DM in the girdled branches that did not find its way into the fruits during the WI period was stored in the branch above the girdle, and was mobilised by the fruits after irrigation was resumed. In all five trials, the relative volume increment was greater than that of the relative DM increment (% S / RI). The fact that the S fruits grew faster than the RI fruits during the post-wi period indicates that the growth potential of the S fruits was not adversely affected during the water-stress periods. To gain some understanding as to what enabled the S fruits to grow faster during the post-wi period, the values for DM/unit volume of these fruits are presented in Table 4. The data in Table 4 show that the final DM/C~' values were similar in S and RI fruits, a situation far different from that existing at the end of the drought period (Table 2). This indicates that the S fruits, when receiving ample post-wi irrigation, were able to utilise a great part of the accumulated DM for volume growth. The fact that values of DM/cm3 were somewhat higher in S fruits, indicates that at least some of the accumulated DM was 'unavailable' for post-wi fruit volume growth. Table 5. Mean It s.e. fruit volume and DM contents at harvest of RI and S fruits from non-girdled and girdled branches in the Bet Dagan trials, 1984 Trial details and sample fruit numbers as in Table Trial ~irdling~ Harvest RI fruits S fruits No. date Volume (cm3) DM (g) Volume (cm3) DM (g) 3 N 30 Oct O.Of N 30 Oct f f1.1 5 G 3 Sept. 197k Of k1.5 6 G 30 Oct f G 30Oct. 278k f A~ = non-girdled branches, G = girdled branches. We have found DM unavailability for fruit volume growth more pronounced in trials where S trees had been under-irrigated, i.e. had received less than the optimal amount of water at every irrigation throughout the whole season. In such trials, grapefruits from trees receiving 0.5RI contained 9-0 and 9.9% more DM/cm3 when borne on nongirdled and girdled branches, respectively. Similarly, in a trial in the 'Shamouti' orange at Ramat Hakovesh in 1983 (Goell and Cohen 1984), the DM/cm3 values for fruit from the 0.5RI treatment were 22% higher than those from RI. Table 4 shows that all fruits from girdled branches contained somewhat more DM /cm3 than those from non-girdled ones, but that the S/RI ratios were about the same. The effects of drought treatments on fruit volume and on DM / cm3 at harvest in fruits from non-girdled and girdled branches are shown in Table 5. At harvest, S fruits on non-girdled branches were cm3 smaller than RI fruits. On girdled branches, the size difference was smaller (4-14 cm3). The same was true for DM contents of the fruits. The fact that S fruits from non-girdled branches accumulated less DM than the RI equivalents may indicate the existence of competition between the fruits and other sinks in the tree. Where such competition does not exist (in girdled branches) the S and RI fruits accumulated similar amounts of DM. This similarity further indicates that the fruits benefited only from the DM produced by the leaves above the girdle, and not from supply of DM from other organs in the tree. All of the above indicate that DM content of the fruit is definitely a practical, reliable indicator as to the fruit final volume (size) at harvest.
6 Aharon Cohen and Ari Goell However, the frequent determination of DM accumulation in the fruits is made difficult by the small daily amounts reaching the fruit, as indicated by the data in Table 6. To estimate daily accumulation of DM accurately, increments for more than 7 days were required. Such a long interval between DM determination is not satisfactory for deciding when to irrigate after a WI period, a decision which needs to be made before long-term fruit volume growth is negatively affected. Further studies have been initiated to overcome this difficulty. The findings presented in this paper seem to conflict with previous reports that photosynthesis is closely related to transpiration (Bielorai and Mendel 1969; Possingham and Kriedemann 1969; Melzack et al. 1985). The results show that, even when no fruit volume growth is discernible (and even some shrinkage can be observed), a condition which implies a low rate of transpiration resulting from decreasing availability of water, DM accumulation continues at a near-normal rate. Working in citrus trees, Cohen et al. (1983) correlated whole-tree transpiration with the rate of water flow in the tree trunk. According to their measurements, the transpiration rate is highest after the trees are irrigated, and remains high for up to 1 week. In the next days it declines gradually, levelling off at a much lower rate for a relatively longer period. Our data show that the rate of DM production and its accumulation in the fruit are hardly affected during very Table 6. Average daily DM accumulation in fruits from RI trees, calculated from periodic DM determinations in fruits from non-girdled and girdled branches Bet Dagan DM ratio (g per fruit) G/ N = Fruit volume ratio (cm3) G / N = Average leaf area / fruit in girdled branches = 970 cm2 Test period Daily DM accumulation (mg/ fruit) Non-girdled Girdled 26 July- 2 Sept Sept.-30 Oct Average (26 July-30 Oct.) long periods of drought, including the period during which transpiration has levelled off at the low rate according to Cohen et al. (1983). Combining these two observations leads to the assumption that the period immediately after each irrigation (even more than 1 week) might be designated as one of 'luxury consumption' of water, since the ratio DM produced / water transpired is much lower in the first period than later on. This concept of 'luxury consumption' of water seems, also, to conflict with previous reports to the effect that photosynthesis is closely related to the rate of transpiration. The present state of limited information calls for further studies to validate the possibility of 'luxury consumption' of water and to resolve the apparent discrepancy with previous observations mentioned above. Summing up the data presented thus far leads to the following conclusions: (1) Drought affects fruit volume growth more severely than it does the accumulation of DM in the fruit. (2) The volume increment rate of the fruit during WI does not necessarily indicate what the final size of the fruit will be, contrary to the conclusion of Oppenheimer and Elze (1941). (3) The excess DM accumulated in the S fruits may well be one of the factors (perhaps the major one) enabling the faster and more prolonged volume growth in S fruits after WI is terminated.
7 Water Stress, Fruit Growth and Dry Matter in Grapefruit (4) In no case in this study did the fruits from S trees reach a larger volume than would be expected of their DM content. This indicates that accumulated DM (in the fruit) plays an important role in determining final fruit size. (5) The use of the rate of DM accumulation in the fruits of S trees as an indicator for the need to irrigate is impracticable at this stage, owing to the small daily increments involved. The importance of the DM production and the resolving of the problem of frequent, accurate DM increment determinations are basic to the further pursuance of this line of research. References Bielorai, H., and Mendel, K. (1969). The simultaneous measurement of apparent photosynthesis and transpiration of citrus seedlings at different moisture levels. J. Am. Soc. Hortic. Sci. 94, Chalmers, D. J., Burge, G., Jerie, P. H., and Mitchell, P. D. (1986). The mechanism of regulation of 'Bartlett' pear fruit and vegetative growth by irrigation withholding and regulated deficit irrigation. J. Am. Soc. Hortic. Sci. 111, Chalmers, D. J., and Wilson, I. B. (1978). Productivity of peach trees: tree growth and water stress in relation to fruit growth and assimilate demand. Ann. Bot. 42, Cohen, A. (1984). Citrus fruit enlargement by means of summer girdling. J. Hortic. Sci. 59, Cohen, A., and Goell, A. (1984). Fruit development as an indicator of the irrigation needs of citrus trees. Proc. Int. Soc. Citriculture Congr. (Brazil) Vol. 1, pp Cohen, A,, Goell, A., Rassiss, A., and Gokkes, M. (1968). Effects of irrigation regimes on grapefruit peel and pulp relationship. Isr. J. Agric. Res. 18, Cohen, Y., Fuchs, M., and Cohen, S. (1983). Resistance to water uptake in a mature citrus orchard. J. Exp. Bot. 34, Furr, J. R., and Taylor, C. A. (1939). Growth of lemon fruits in relation to moisture contents of the soil. USDA Tech. Bull. No Goell, A. (1972). (Considerations and thoughts on irrigating citrus orchards. Part 11. Fruit quality effects.) Alon Hanotea 26, (In Hebrew). Goell, A., and Cohen, A. (1981). Combining irrigation regimes with girdling techniques in citrus trees (a new experimental mode). Proc. Int. Soc. Citriculture Congr. (Japan) Vol. 2, pp Goell, A., and Cohen, A. (1984). Determining irrigation requirements of girdled citrus trees by means of the "Graduated Irrigation" experimental mode. Proc. Int. Soc. Citriculture Congr. (Brazil) Vol. 1, pp Goell, A., Golomb, A., Kalmar, D., Mantell, A., and Sharon Sh. (1981). Moisture stress - a potent factor for affecting vegetative growth and tree size in citrus. Proc. Int. Soc. Citriculture Congr. (Japan) Vol. 2, pp Goell, A., and Levy, Y. (1970). The effects of irrigation stress on fruit quality. Proc. 18th Int. Hortic. Congr. (Israel) Abstr. 449, Vol. 1, pp McNulty, I. B. (1985). Rapid osmotic adjustment by a succulent halophyte to saline shock. Plant Physiol. 78, Melzack, R. N., Bravdo, B., and Riov, J. (1985). The effect of water stress on photosynthesis and related parameters in Pinus halepensis. Physiol. Plant. 64, Mitchell, P. D., Chalmers, D. J., Jerie, P. H., and Burge, G. (1986). The use of initial withholding of irrigation and tree spacing to enhance the effect of regulated deficit irrigation on pear trees. J. Am. SOC. Hortic. Sci. 111, Oppenheimer, R. H., and Elze, D. L. (1941). Irrigation of citrus trees according to physiological indicators. Rehovot, Israel, Agric. Res. Stn. Bull. No. 31. Possingham, J. V., and Kriedemann, P. E. (1969). Environmental effects on the formation and distribution of photosynthetic assimilates in citrus. Proc. First Int. Citrus Symp. (U.S.A.) Vol. 1, pp (Ed. H. D. Chapman.) Turrell, F. M. (1946). 'Tables of Surfaces and Volumes of Spheres and of Prolate and Oblate Spheroids.' (University of California Press: Berkeley.) Yelenosky, G. (1978). Cold hardening 'Valencia' orange trees to tolerate - 6-7OC without injury. J. Am. Soc. Hortic. Sci. 193, Manuscript received 27 March 1986, accepted 30 June 1988
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